Abstract
Rough-skinned newts (Taricha granulosa) use tetrodotoxin (TTX) to block voltage-gated sodium (Nav) channels as a chemical defense against predation. Interestingly, newts exhibit extreme population-level variation in toxicity attributed to a coevolutionary arms race with TTX-resistant predatory snakes, but the source of TTX in newts is unknown. Here, we investigated whether symbiotic bacteria isolated from toxic newts could produce TTX. We characterized the skin-associated microbiota from a toxic and non-toxic population of newts and established pure cultures of isolated bacterial symbionts from toxic newts. We then screened bacterial culture media for TTX using LC-MS/MS and identified TTX-producing bacterial strains from four genera, including Aeromonas, Pseudomonas, Shewanella, and Sphingopyxis. Additionally, we sequenced the Nav channel gene family in toxic newts and found that newts expressed Nav channels with modified TTX binding sites, conferring extreme physiological resistance to TTX. This study highlights the complex interactions among adaptive physiology, animal-bacterial symbiosis, and ecological context.
Highlights
Coevolutionary interactions among species are a central force driving the origin of novel, adaptive phenotypes, yet the traits under selection are often complex and arise from multifaceted interactions among genetic, physiological, and environmental forces that are not well understood (Ehrlich and Raven, 1964; Futuyma and Agrawal, 2009; Schoener, 2011)
Scanning electron micrographs of dorsal granular glands revealed the presence of bacteria inhabiting the surface and outer pore of TTX-sequestering granular glands, and mixed bacterial communities including rod and coccus-shaped bacterial cells were present within the ducts of these glands
We found that bacterial isolates from four genera, Aeromonas, Pseudomonas, Shewanella, and Sphingopyxis, cultured from the skin of T. granulosa produce TTX under laboratory conditions
Summary
Coevolutionary interactions among species are a central force driving the origin of novel, adaptive phenotypes, yet the traits under selection are often complex and arise from multifaceted interactions among genetic, physiological, and environmental forces that are not well understood (Ehrlich and Raven, 1964; Futuyma and Agrawal, 2009; Schoener, 2011). Vaelli et al looked at five genes that encode the channels normally affected by TTX in newts and found that all them have mutations that prevent them from being blocked by this deadly neurotoxin This suggests that bacteria living on newts shape the evolution of genes critical to the animals’ own survival. Rough-skinned newts (Taricha granulosa) are among the most poisonous TTX-producing animals and serve as an excellent model system for understanding ecological influences on toxin production and predation (Figure 1A). This species is endemic to the Pacific Northwest of North America, where certain populations possess high quantities of TTX relative to other TTX-laden species including pufferfishes and blue-ringed octopuses (Hanifin, 2010; Williams, 2010). Our results suggest that host-associated bacteria may underlie the production of a critical defensive compound in a vertebrate host, impacting predator-prey coevolution and potentially shaping the evolution of TTX resistance in a well-known ecological model system
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